We used mitochondrial DNA sequence data and 12 microsatellite loci to examine the genetic structure of Cotesia melitaearum (Wilkinson) (Hymenoptera: Braconidae), a parasitoid wasp reared from two common butterfly species, Melitaea cinxia (L.) (Lepidoptera: Nymphalidae) and Euphydryas aurinia (Rottemburg) (Lepidoptera: Nymphalidae), across many localities in Europe and Asia, as well as from four more narrowly distributed related European species. The haplotypes of wasps reared from M. cinxia and E. aurinia show a complex geographic pattern presumably reflecting long-term history, but the microsatellite data yield two host-associated groups, each including populations across Europe and suggesting that currently there is no gene flow between the parasitoid populations attacking these two widely distributed host species. The cryptic species attacking E. aurinia also parasitizes the closely related Euphydryas desfontainii (Godart), but the three remaining host species have yet another, or possibly several, previously unrecognized parasitoid species. We support the cryptic species status of two C. melitaearum aggregate forms parasitizing M. cinxia and Melitaea athalia (Rottemburg) in the Åland Islands in Finland and provide behavioral and ecological data in addition to the molecular data.